Rapid turnover of apolipoprotein C-III-containing triglyceride-rich lipoproteins contributing to the formation of LDL subfractions

Journal of Lipid Research

Volumn 48, Issue 5, 2007, Pages 1190-1203

  Zheng, Chunyu ^a   Khoo, Christina ^a,c   Ikewaki, Katsunori ^b   Sacks, Frank M ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Hill's Pet Nutrition Inc   (United States)

Author keywords

Apolipoprotein B 100; Apolipoprotein E; Kinetics; Low density lipoprotein; Stable isotopes

Indexed keywords

APOLIPOPROTEIN B; APOLIPOPROTEIN C1; APOLIPOPROTEIN C2; APOLIPOPROTEIN C3; APOLIPOPROTEIN E; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

ADULT; AGED; ARTICLE; ATHEROGENESIS; CLINICAL ARTICLE; CONTROLLED STUDY; DEMOGRAPHY; DYSLIPIDEMIA; FEMALE; HUMAN; HYPERTRIGLYCERIDEMIA; LIPID BLOOD LEVEL; LIPID METABOLISM; LIPOGENESIS; LIPOLYSIS; LIPOPROTEIN METABOLISM; LIVER CLEARANCE; MALE; PRIORITY JOURNAL; PROTEIN DEGRADATION;

APOLIPOPROTEIN C-III; APOLIPOPROTEINS E; CHOLESTEROL, LDL; CHOLESTEROL, VLDL; FEMALE; HUMANS; HYPERTRIGLYCERIDEMIA; LIVER; MALE; MIDDLE AGED; TIME FACTORS; TRIGLYCERIDES;

EID: 34248172313     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.P600011-JLR200     Document Type: Article

References (46)

1. Alaupovic, P., W. J. Mack, C. Knight-Gibson, and H. N. Hodis. 1997. The role of triglyceride-rich lipoprotein families in the progression of atherosclerotic lesions as determined by sequential coronary angiography from a controlled clinical trial. Arterioscler. Thromb. Vasc. Biol. 17: 715-722.
2. Sacks, F. M., P. Alaupovic, L. A. Moye, T. G. Cole, B. Sussex, M. J. Stampfer, M. A. Pfeffer, and E. Braunwald. 2000. VLDL, apolipoproteins B, CIII, and E, and risk of recurrent coronary events in the Cholesterol and Recurrent Events (CARE) Trial. Circulation. 102: 1886-1892.
3. Lee, S. J., H. Campos, L. A. Moye, and F. M. Sacks. 2003. LDL containing apolipoprotein CIII is an independent risk factor for coronary events in diabetic patients. Arterioscler. Thromb. Vasc. Biol. 23: 853-858.
4. Alaupovic, P. 1996. Significance of apolipoproteins for structure, function, and classification of plasma lipoproteins. Methods Enzymol. 263: 32-60.
5. Campos, H., D. Perlov, C. Khoo, and F. M. Sacks. 2001. Distinct patterns of lipoproteins with apoB defined by presence of apoE or apoC-III in hypercholesterolemia and hypertriglyceridemia. J. Lipid Res. 42: 1239-1249.
6. Khoo, C., H. Campos, H. Judge, and F. M. Sacks. 1999. Effects of estrogenic oral contraceptives on the lipoprotein B particle system defined by apolipoproteinsE andC-III content. J. Lipid Res. 40: 202-212.
7. Brown, W. V., and M. L. Baginsky. 1972. Inhibition of lipoprotein lipase by an apoprotein of human very low density lipoprotein. Biochem. Biophys. Res. Commun. 46: 375-382.
8. Wang, C. S., W. J. McConathy, H. U. Kloer, and P. Alaupovic. 1985. Modulation of lipoprotein lipase activity by apolipoproteins. Effect of apolipoprotein C-III. J. Clin. Invest. 75: 384-390.
9. Kinnunen, P. K., and C. Ehnolm. 1976. Effect of serum and C-apoproteins from very low density lipoproteins on human post-heparin plasma hepatic lipase. FEBS Lett. 65: 354-357.
10. Clavey, V., S. Lestavel-Delattre, C. Copin, J. M. Bard, and J. C. Fruchart. 1995. Modulation of lipoprotein B binding to the LDL receptor by exogenous lipids and apolipoproteins CI, CII, CIII, and E. Arterioscler. Thromb. Vasc. Biol. 15: 963-971.
11. Windler, E. E., P. T. Kovanen, Y. S. Chao, M. S. Brown, R. J. Havel, and J. L. Goldstein. 1980. The estradiol-stimulated lipoprotein receptor of rat liver. A binding site that membrane mediates the uptake of rat lipoproteins containing apoproteins B and E. J. Biol. Chem. 255: 10464-10471.
12. Sehayek, E., and S. Eisenberg. 1991. Mechanisms of inhibition by apolipoprotein C of apolipoprotein E-dependent cellular metabolism of human triglyceride-rich lipoproteins through the low density lipoprotein receptor pathway. J. Biol. Chem. 266: 18259-18267.
13. Ito, Y., N. Azrolan, A. O'Connell, A. Walsh, and J. L. Breslow. 1990. Hypertriglyceridemia as a result of human apo CIII gene expression in transgenic mice. Science. 249: 790-793.
14. Aalto-Setala, K., E. A. Fisher, X. Chen, T. Chajek-Shaul, T. Hayek, R. Zechner, A. Walsh, R. Ramakrishnan, H. N. Ginsberg, and J. L. Breslow. 1992. Mechanism of hypertriglyceridemia in human apolipoprotein (apo) CIII transgenic mice. Diminished very low density lipoprotein fractional catabolic rate associated with increased apo CIII and reduced apo E on the particles. J. Clin. Invest. 90: 1889-1900.
15. Aalto-Setala, K., P. H. Weinstock, C. L. Bisgaier, L. Wu, J. D. Smith, and J. L. Breslow. 1996. Further characterization of the metabolic properties of triglyceride-rich lipoproteins from human and mouse apoC-III transgenic mice. J. Lipid Res. 37: 1802-1811.
16. de Silva, H. V., S. J. Lauer, J. Wang, W. S. Simonet, K. H. Weisgraber, R. W. Mahley, and J. M. Taylor. 1994. Overexpression of human apolipoprotein C-III in transgenic mice results in an accumulation of apolipoprotein B48 remnants that is corrected by excess apolipoprotein E. J. Biol. Chem. 269: 2324-2335.
17. Ebara, T., R. Ramakrishnan, G. Steiner, and N. S. Shachter. 1997. Chylomicronemia due to apolipoprotein CIII overexpression in apolipoprotein E-null mice. Apolipoprotein CIII-induced hypertriglyceridemia is not mediated by effects on apolipoprotein E. J. Clin. Invest. 99: 2672-2681.
18. Maeda, N., H. Li, D. Lee, P. Oliver, S. H. Quarfordt, and J. Osada. 1994. Targeted disruption of the apolipoprotein C-III gene in mice results in hypotriglyceridemia and protection from postprandial hypertriglyceridemia. J. Biol. Chem. 269: 23610-23616.
19. Jong, M. C., P. C. Rensen, V. E. Dahlmans, H. van der Boom, T. J. van Berkel, and L. M. Havekes. 2001. Apolipoprotein C-III deficiency accelerates triglyceride hydrolysis by lipoprotein lipase in wild-type and apoE knockout mice. J. Lipid Res. 42: 1578-1585.
20. Ginsberg, H. N., N. A. Le, I. J. Goldberg, J. C. Gibson, A. Rubinstein, P. Wang-Iverson, R. Norum, and W. V. Brown. 1986. Apolipoprotein B metabolism in subjects with deficiency of apolipoproteins CIII and AI. Evidence that apolipoprotein CIII inhibits catabolism of triglyceride-rich lipoproteins by lipoprotein lipase in vivo. J. Clin. Invest. 78: 1287-1295.
21. Cohn, J. S., B. W. Patterson, K. D. Uffelman, J. Davignon, and G. Steiner. 2004. Rate of production of plasma and very-low-density lipoprotein (VLDL) apolipoprotein C-III is strongly related to the concentration and level of production of VLDL triglyceride in male subjects with different body weights and levels of insulin sensitivity. J. Clin. Endocrinol. Metab. 89: 3949-3955.
22. Chan, D. C., G. F. Watts, M. N. Nguyen, and P. H. Barrett. 2006. Apolipoproteins C-III and A-V as predictors of very-low-density lipoprotein triglyceride and apolipoprotein B-100 kinetics. Arterioscler. Thromb. Vasc. Biol. 26: 590-596.
23. Kowal, R. C., J. Herz, K. H. Weisgraber, R. W. Mahley, M. S. Brown, and J. L. Goldstein. 1990. Opposing effects of apolipoproteins E and C on lipoprotein binding to low density lipoprotein receptor-related protein. J. Biol. Chem. 265: 10771-10779.
24. Mahley, R. W., and S. C. Rall, Jr. 2000. Apolipoprotein E: far more than a lipid transport protein. Annu. Rev. Genomics Hum. Genet. 1: 507-537.
25. Ji, Z. S., S. Fazio, Y. L. Lee, and R. W. Mahley. 1994. Secretion-capture role for apolipoprotein E in remnant lipoprotein metabolism involving cell surface heparan sulfate proteoglycans. J. Biol. Chem. 269: 2764-2772.
26. Ikewaki, K., W. Cain, F. Thomas, R. Shamburek, L. A. Zech, D. Usher, H. B. Brewer, Jr., and D. J. Rader. 2004. Abnormal in vivo metabolism of apoB-containing lipoproteins in human apoE deficiency. J. Lipid Res. 45: 1302-1311.
27. Schaefer, E. J., R. E. Gregg, G. Ghiselli, T. M. Forte, J. M. Ordovas, L. A. Zech, and H. B. Brewer, Jr. 1986. Familial apolipoprotein E deficiency. J. Clin. Invest. 78: 1206-1219.
28. Tomiyasu, K., B. W. Walsh, K. Ikewaki, H. Judge, and F. M. Sacks. 2001. Differential metabolism of human VLDL according to content of apoE and apoC-III. Arterioscler. Thromb. Vasc. Biol. 21: 1494-1500.
29. Kawakami, A., M. Aikawa, P. Alcaide, F. W. Luscinskas, P. Libby, and F. M. Sacks. 2006. Apolipoprotein CIII induces expression of vascular cell adhesion molecule-1 in vascular endothelial cells and increases adhesion of monocytic cells. Circulation. 114: 681-687.
30. Kawakami, A., M. Aikawa, P. Libby, P. Alcaide, F. W. Luscinskas, and F. M. Sacks. 2006. Apolipoprotein CIII in apolipoprotein B lipoproteins enhances the adhesion of human monocytic cells to endothelial cells. Circulation. 113: 691-700.
31. Kawakami, A., M. Aikawa, N. Nitta, M. Yoshida, P. Libby, and F. M. Sacks. 2007. Apolipoprotein CIII-induced THP-1 cell adhesion to endothelial cells involves pertussis toxin-sensitive G protein- and protein kinase Calpha-mediated nuclear factor-kappaB activation. Arterioscler. Thromb. Vasc. Biol. 27: 219-225.
32. Lindgren, F. T., L. C. Jensen, and F. T. Hatch. 1972. The isolation and quantitative analysis of serum lipoproteins. In Blood Lipids and Lipoproteins: Quantitation, Composition, and Metabolism. G. J. Nelson, editor. John Wiley-Interscience, New York. 181-274.
33. Ehnholm, C., H. Garoff, K. Simons, and H. Aro. 1971. Purification and quantitation of the human plasma lipoprotein carrying the Lp(a) antigen. Biochim. Biophys. Acta. 236: 431-439.
34. Su, W., H. Campos, H. Judge, B. W. Walsh, and F. M. Sacks. 1998. Metabolism of apo(a) and apoB100 of lipoprotein(a) in women: effect of postmenopausal estrogen replacement. J. Clin. Endocrinol. Metab. 83: 3267-3276.
35. Maugeais, C., K. Ouguerram, R. Frenais, P. Maugere, B. Charbonnel, T. Magot, and M. Krempf. 2001. Effect of low-density lipoprotein apheresis on kinetics of apolipoprotein B in heterozygous familial hypercholesterolemia. J. Clin. Endocrinol. Metab. 86: 1679-1686.
36. Olin-Lewis, K., R. M. Krauss, M. La Belle, P. J. Blanche, P. H. Barrett, T. N. Wight, and A. Chait. 2002. ApoC-III content of apoBcontaining lipoproteins is associated with binding to the vascular proteoglycan biglycan. J. Lipid Res. 43: 1969-1977.
37. Fisher, W. R., L. A. Zech, P. Bardalaye, G. Warmke, and M. Berman. 1980. The metabolism of apolipoprotein B in subjects with hypertriglyceridemia and polydisperse LDL. J. Lipid Res. 21: 760-774.
38. Dunn, F. L., S. M. Grundy, D. W. Bilheimer, R. J. Havel, and P. Raskin. 1985. Impaired catabolism of very low-density lipoproteintriglyceride in a family with primary hypertriglyceridemia. Metabolism. 34: 316-324.
39. Nguyen, M. N., D. C. Chan, K. P. Dwyer, P. Bolitho, G. F. Watts, and P. H. Barrett. 2006. Use of Intralipid for kinetic analysis of HDL apoC-III: evidence for a homogeneous kinetic pool of apoC-III in plasma. J. Lipid Res. 47: 1274-1280.
40. Blum, C. B. 1982. Dynamics of apolipoprotein E metabolism in humans. J. Lipid Res. 23: 1308-1316.
41. Abbott, W. G., B. Swinburn, G. Ruotolo, H. Hara, L. Patti, I. Harper, S. M. Grundy, and B. V. Howard. 1990. Effect of a high-carbohydrate, low-saturated-fat diet on apolipoprotein B and triglyceride metabolism in Pima Indians. J. Clin. Invest. 86: 642-650.
42. Batal, R., M. Tremblay, P. H. Barrett, H. Jacques, A. Fredenrich, O. Mamer, J. Davignon, and J. S. Cohn. 2000. Plasma kinetics of apoC-III and apoE in normolipidemic and hypertriglyceridemic subjects. J. Lipid Res. 41: 706-718.
43. Bukberg, P. R., N. A. Le, H. N. Ginsberg, J. C. Gibson, A. Rubinstein, and W. V. Brown. 1985. Evidence for non-equilibrating pools of apolipoprotein C-III in plasma lipoproteins. J. Lipid Res. 26: 1047-1057.
44. Huff, M. W., and P. J. Nestel. 1982. Metabolism of apolipoproteins CII, CIII1, CIII2 and VLDL-B in human subjects consuming high carbohydrate diets. Metabolism. 31: 493-498.
45. Dong, L. M., C. Wilson, M. R. Wardell, T. Simmons, R. W. Mahley, K. H. Weisgraber, and D. A. Agard. 1994. Human apolipoprotein E. Role of arginine 61 in mediating the lipoprotein preferences of the E3 and E4 isoforms. J. Biol. Chem. 269: 22358-22365.
46. Shachter, N. S. 2001. Apolipoproteins C-I and C-III as important modulators of lipoprotein metabolism. Curr. Opin. Lipidol. 12: 297-304.